This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Campbell, B. J.
Right arrow Articles by Cary, S. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Campbell, B. J.
Right arrow Articles by Cary, S. C.
Agricola
Right arrow Articles by Campbell, B. J.
Right arrow Articles by Cary, S. C.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, October 2001, p. 4566-4572, Vol. 67, No. 10
0099-2240/01/$04.00+0   DOI: 10.1128/AEM.67.10.4566-4572.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Growth and Phylogenetic Properties of Novel Bacteria Belonging to the Epsilon Subdivision of the Proteobacteria Enriched from Alvinella pompejana and Deep-Sea Hydrothermal Vents

Barbara J. Campbell,1 Christian Jeanthon,2 Joel E. Kostka,3 George W. Luther III,1 and S. Craig Cary1,*

College of Marine Studies, University of Delaware, Lewes, Delaware 199581; UMR6539, Centre National de la Recherche Scientifique and Université de Bretagne Occidentale, 29280 Plouzané, France2; and Department of Oceanography, Florida State University, Tallahassee, Florida 323063

Received 20 March 2001/Accepted 4 July 2001

Recent molecular characterizations of microbial communities from deep-sea hydrothermal sites indicate the predominance of bacteria belonging to the epsilon subdivision of Proteobacteria (epsilon Proteobacteria). Here, we report the first enrichments and characterizations of four epsilon Proteobacteria that are directly associated with Alvinella pompejana, a deep sea hydrothermal vent polychete, or with hydrothermal vent chimney samples. These novel bacteria were moderately thermophilic sulfur-reducing heterotrophs growing on formate as the energy and carbon source. In addition, two of them (Am-H and Ex-18.2) could grow on sulfur lithoautrotrophically using hydrogen as the electron donor. Optimal growth temperatures of the bacteria ranged from 41 to 45°C. Phylogenetic analysis of the small-subunit ribosomal gene of the two heterotrophic bacteria demonstrated 95% similarity to Sulfurospirillum arcachonense, an epsilon Proteobacteria isolated from an oxidized marine surface sediment. The autotrophic bacteria grouped within a deeply branching clade of the epsilon Proteobacteria, to date composed only of uncultured bacteria detected in a sample from a hydrothermal vent along the mid-Atlantic ridge. A molecular survey of various hydrothermal vent environments demonstrated the presence of two of these bacteria (Am-N and Am-H) in more than one geographic location and habitat. These results suggest that certain epsilon Proteobacteria likely fill important niches in the environmental habitats of deep-sea hydrothermal vents, where they contribute to overall carbon and sulfur cycling at moderate thermophilic temperatures.


* Corresponding author. Mailing address: College of Marine Studies, University of Delaware, Lewes, DE 19958. Phone: (302) 645-4078. Fax: (302) 645-4007, E-mail: caryc{at}udel.edu.


Applied and Environmental Microbiology, October 2001, p. 4566-4572, Vol. 67, No. 10
0099-2240/01/$04.00+0   DOI: 10.1128/AEM.67.10.4566-4572.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Alain, K., Callac, N., Guegan, M., Lesongeur, F., Crassous, P., Cambon-Bonavita, M.-A., Querellou, J., Prieur, D. (2009). Nautilia abyssi sp. nov., a thermophilic, chemolithoautotrophic, sulfur-reducing bacterium isolated from an East Pacific Rise hydrothermal vent. Int. J. Syst. Evol. Microbiol. 59: 1310-1315 [Abstract] [Full Text]  
  • Smith, J. L., Campbell, B. J., Hanson, T. E., Zhang, C. L., Cary, S. C. (2008). Nautilia profundicola sp. nov., a thermophilic, sulfur-reducing epsilonproteobacterium from deep-sea hydrothermal vents. Int. J. Syst. Evol. Microbiol. 58: 1598-1602 [Abstract] [Full Text]  
  • Nyholm, S. V., Robidart, J., Girguis, P. R. (2008). Coupling Metabolite Flux to Transcriptomics: Insights Into the Molecular Mechanisms Underlying Primary Productivity by the Hydrothermal Vent Tubeworm Ridgeia piscesae. Biol. Bull. 214: 255-265 [Abstract] [Full Text]  
  • Lee, C. K., Cary, S. C., Murray, A. E., Daniel, R. M. (2008). Enzymic Approach to Eurythermalism of Alvinella pompejana and Its Episymbionts. Appl. Environ. Microbiol. 74: 774-782 [Abstract] [Full Text]  
  • Crapart, S., Fardeau, M.-L., Cayol, J.-L., Thomas, P., Sery, C., Ollivier, B., Combet-Blanc, Y. (2007). Exiguobacterium profundum sp. nov., a moderately thermophilic, lactic acid-producing bacterium isolated from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 57: 287-292 [Abstract] [Full Text]  
  • Sogin, M. L., Morrison, H. G., Huber, J. A., Welch, D. M., Huse, S. M., Neal, P. R., Arrieta, J. M., Herndl, G. J. (2006). Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Natl. Acad. Sci. USA 103: 12115-12120 [Abstract] [Full Text]  
  • Takai, K., Suzuki, M., Nakagawa, S., Miyazaki, M., Suzuki, Y., Inagaki, F., Horikoshi, K. (2006). Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas.. Int. J. Syst. Evol. Microbiol. 56: 1725-1733 [Abstract] [Full Text]  
  • Lin, X., Wakeham, S. G., Putnam, I. F., Astor, Y. M., Scranton, M. I., Chistoserdov, A. Y., Taylor, G. T. (2006). Comparison of Vertical Distributions of Prokaryotic Assemblages in the Anoxic Cariaco Basin and Black Sea by Use of Fluorescence In Situ Hybridization. Appl. Environ. Microbiol. 72: 2679-2690 [Abstract] [Full Text]  
  • Brettar, I., Labrenz, M., Flavier, S., Botel, J., Kuosa, H., Christen, R., Hofle, M. G. (2006). Identification of a Thiomicrospira denitrificans-Like Epsilonproteobacterium as a Catalyst for Autotrophic Denitrification in the Central Baltic Sea. Appl. Environ. Microbiol. 72: 1364-1372 [Abstract] [Full Text]  
  • Takai, K., Campbell, B. J., Cary, S. C., Suzuki, M., Oida, H., Nunoura, T., Hirayama, H., Nakagawa, S., Suzuki, Y., Inagaki, F., Horikoshi, K. (2005). Enzymatic and Genetic Characterization of Carbon and Energy Metabolisms by Deep-Sea Hydrothermal Chemolithoautotrophic Isolates of Epsilonproteobacteria. Appl. Environ. Microbiol. 71: 7310-7320 [Abstract] [Full Text]  
  • Hugler, M., Wirsen, C. O., Fuchs, G., Taylor, C. D., Sievert, S. M. (2005). Evidence for Autotrophic CO2 Fixation via the Reductive Tricarboxylic Acid Cycle by Members of the {varepsilon} Subdivision of Proteobacteria. J. Bacteriol. 187: 3020-3027 [Abstract] [Full Text]  
  • Voordeckers, J. W., Starovoytov, V., Vetriani, C. (2005). Caminibacter mediatlanticus sp. nov., a thermophilic, chemolithoautotrophic, nitrate-ammonifying bacterium isolated from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. Int. J. Syst. Evol. Microbiol. 55: 773-779 [Abstract] [Full Text]  
  • Takai, K., Hirayama, H., Nakagawa, T., Suzuki, Y., Nealson, K. H., Horikoshi, K. (2005). Lebetimonas acidiphila gen. nov., sp. nov., a novel thermophilic, acidophilic, hydrogen-oxidizing chemolithoautotroph within the 'Epsilonproteobacteria', isolated from a deep-sea hydrothermal fumarole in the Mariana Arc. Int. J. Syst. Evol. Microbiol. 55: 183-189 [Abstract] [Full Text]  
  • Campbell, B. J., Cary, S. C. (2004). Abundance of Reverse Tricarboxylic Acid Cycle Genes in Free-Living Microorganisms at Deep-Sea Hydrothermal Vents. Appl. Environ. Microbiol. 70: 6282-6289 [Abstract] [Full Text]  
  • Inagaki, F., Takai, K., Nealson, K. H., Horikoshi, K. (2004). Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the {varepsilon}-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int. J. Syst. Evol. Microbiol. 54: 1477-1482 [Abstract] [Full Text]  
  • Koizumi, Y., Kojima, H., Fukui, M. (2004). Dominant Microbial Composition and Its Vertical Distribution in Saline Meromictic Lake Kaiike (Japan) as Revealed by Quantitative Oligonucleotide Probe Membrane Hybridization. Appl. Environ. Microbiol. 70: 4930-4940 [Abstract] [Full Text]  
  • Goffredi, S. K., Waren, A., Orphan, V. J., Van Dover, C. L., Vrijenhoek, R. C. (2004). Novel Forms of Structural Integration between Microbes and a Hydrothermal Vent Gastropod from the Indian Ocean. Appl. Environ. Microbiol. 70: 3082-3090 [Abstract] [Full Text]  
  • Sunamura, M., Higashi, Y., Miyako, C., Ishibashi, J.-i., Maruyama, A. (2004). Two Bacteria Phylotypes Are Predominant in the Suiyo Seamount Hydrothermal Plume. Appl. Environ. Microbiol. 70: 1190-1198 [Abstract] [Full Text]  
  • Takai, K., Nealson, K. H., Horikoshi, K. (2004). Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the {varepsilon}-Proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field. Int. J. Syst. Evol. Microbiol. 54: 25-32 [Abstract] [Full Text]  
  • Miroshnichenko, M. L., L'Haridon, S., Schumann, P., Spring, S., Bonch-Osmolovskaya, E. A., Jeanthon, C., Stackebrandt, E. (2004). Caminibacter profundus sp. nov., a novel thermophile of Nautiliales ord. nov. within the class 'Epsilonproteobacteria', isolated from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 54: 41-45 [Abstract] [Full Text]  
  • Inagaki, F., Takai, K., Kobayashi, H., Nealson, K. H., Horikoshi, K. (2003). Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing {varepsilon}-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 53: 1801-1805 [Abstract] [Full Text]  
  • Campbell, B. J., Stein, J. L., Cary, S. C. (2003). Evidence of Chemolithoautotrophy in the Bacterial Community Associated with Alvinella pompejana, a Hydrothermal Vent Polychaete. Appl. Environ. Microbiol. 69: 5070-5078 [Abstract] [Full Text]  
  • Zhu, X. Y., Lubeck, J., Kilbane, J. J. II (2003). Characterization of Microbial Communities in Gas Industry Pipelines. Appl. Environ. Microbiol. 69: 5354-5363 [Abstract] [Full Text]  
  • Engel, A. S., Lee, N., Porter, M. L., Stern, L. A., Bennett, P. C., Wagner, M. (2003). Filamentous "Epsilonproteobacteria" Dominate Microbial Mats from Sulfidic Cave Springs. Appl. Environ. Microbiol. 69: 5503-5511 [Abstract] [Full Text]  
  • Brisbarre, N., Fardeau, M.-L., Cueff, V., Cayol, J.-L., Barbier, G., Cilia, V., Ravot, G., Thomas, P., Garcia, J.-L., Ollivier, B. (2003). Clostridium caminithermale sp. nov., a slightly halophilic and moderately thermophilic bacterium isolated from an Atlantic deep-sea hydrothermal chimney. Int. J. Syst. Evol. Microbiol. 53: 1043-1049 [Abstract] [Full Text]  
  • Alazard, D., Dukan, S., Urios, A., Verhe, F., Bouabida, N., Morel, F., Thomas, P., Garcia, J.-L., Ollivier, B. (2003). Desulfovibrio hydrothermalis sp. nov., a novel sulfate-reducing bacterium isolated from hydrothermal vents. Int. J. Syst. Evol. Microbiol. 53: 173-178 [Abstract] [Full Text]  
  • Podar, M., Mullineaux, L., Huang, H.-R., Perlman, P. S., Sogin, M. L. (2002). Bacterial Group II Introns in a Deep-Sea Hydrothermal Vent Environment. Appl. Environ. Microbiol. 68: 6392-6398 [Abstract] [Full Text]  
  • Takai, K., Hirayama, H., Sakihama, Y., Inagaki, F., Yamato, Y., Horikoshi, K. (2002). Isolation and Metabolic Characteristics of Previously Uncultured Members of the Order Aquificales in a Subsurface Gold Mine. Appl. Environ. Microbiol. 68: 3046-3054 [Abstract] [Full Text]  
  • Reysenbach, A.-L., Shock, E. (2002). Merging Genomes with Geochemistry in Hydrothermal Ecosystems. Science 296: 1077-1082 [Abstract] [Full Text]